Elasticity and physico-chemical properties during drinking water biofilm formation

Atomic force microscope techniques and multi-staining fluorescence microscopy were employed to study the steps in drinking water biofilm formation. During the formation of a conditioning layer, surface hydrophobic forces increased and the range of characteristic hydrophobic forces diversified with time, becoming progressively complex in macromolecular composition, which in return triggered irreversible cellular adhesion. AFM visualization of 1 to 8 week drinking water biofilms showed a spatially discontinuous and heterogeneous distribution comprising an extensive network of filamentous fungi in which biofilm aggregates were embedded. The elastic modulus of 40-day-old biofilms ranged from 200 to 9000 kPa, and the biofilm deposits with a height >0.5 μm had an elastic modulus <600 kPa, suggesting that the drinking water biofilms were composed of a soft top layer and a basal layer with significantly higher elastic modulus values falling in the range of fungal elasticity.

[1]  S. Kjelleberg,et al.  The biofilm mode of life : mechanisms and adaptations , 2007 .

[2]  J. Wingender,et al.  Chemical and physical methods for characterisation of biofilms , 2007 .

[3]  O. Sire,et al.  Does water activity rule P. mirabilis periodic swarming? I. Biochemical and functional properties of the extracellular matrix. , 2007, Biomacromolecules.

[4]  Jeremy S. Webb,et al.  Enhanced Biofilm Formation and Increased Resistance to Antimicrobial Agents and Bacterial Invasion Are Caused by Synergistic Interactions in Multispecies Biofilms , 2006, Applied and Environmental Microbiology.

[5]  Hertz On the Contact of Elastic Solids , 1882 .

[6]  Hideki Harada,et al.  A novel method for evaluation of biofilm tensile strength resisting erosion , 1999 .

[7]  S. B. Surman,et al.  Comparison of microscope techniques for the examination of biofilms , 1996 .

[8]  F. Tay,et al.  Role of Silver Ions in Destabilization of Intermolecular Adhesion Forces Measured by Atomic Force Microscopy in Staphylococcus epidermidis Biofilms , 2005, Antimicrobial Agents and Chemotherapy.

[9]  Anand Jain,et al.  Biochemical composition of the marine conditioning film: implications for bacterial adhesion , 2009, Biofouling.

[10]  Y. Lévi,et al.  Biofilm accumulation in drinking water distribution systems , 1993 .

[11]  H. Hansma,et al.  Elongation Correlates with Nutrient Deprivation in Pseudomonas aeruginosa Unsaturated Biofilms , 2002, Microbial Ecology.

[12]  Yves F Dufrêne,et al.  Atomic force microscopy of microbial cells: application to nanomechanical properties, surface forces and molecular recognition forces. , 2007, Colloids and surfaces. B, Biointerfaces.

[13]  J. Keener,et al.  The role of the biofilm matrix in structural development. , 2004, Mathematical medicine and biology : a journal of the IMA.

[14]  Eileen M. Spain,et al.  Spring constants and adhesive properties of native bacterial biofilm cells measured by atomic force microscopy. , 2008, Colloids and surfaces. B, Biointerfaces.

[15]  S. Percival,et al.  Potable water and biofilms: A review of the public health implications , 1999 .

[16]  Bernard Nysten,et al.  Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy , 2003 .

[17]  Y. Oh,et al.  Effects of substrates on biofilm formation observed by atomic force microscopy. , 2009, Ultramicroscopy.

[18]  Yves F Dufrêne,et al.  Chemical force microscopy of single live cells. , 2007, Nano letters.

[19]  A. Steele,et al.  The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces , 2002 .

[20]  Yves F Dufrêne,et al.  Direct measurement of hydrophobic forces on cell surfaces using AFM. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[21]  H. C. van der Mei,et al.  Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. , 2008, Microbiology.

[22]  Karsten Pedersen,et al.  Biofilm development on stainless steel and PVC surfaces in drinking water , 1990 .

[23]  S. Sharma,et al.  Influence of surface properties on accumulation of conditioning films and marine bacteria on substrata exposed to oligotrophic waters , 1997 .

[24]  I. Klapper,et al.  Role of cohesion in the material description of biofilms. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  R. Schneider Bacterial adhesion to solid substrata coated with conditioning films derived from chemical fractions of natural waters , 1997 .

[26]  B. Harrington,et al.  Calcofluor White: A Review of its Uses and Applications in Clinical Mycology and Parasitology , 2003 .

[27]  H. Hertz Ueber die Berührung fester elastischer Körper. , 1882 .

[28]  Janshoff,et al.  Force Spectroscopy of Molecular Systems-Single Molecule Spectroscopy of Polymers and Biomolecules. , 2000, Angewandte Chemie.

[29]  P. Richardson,et al.  Principles of Cell Adhesion , 1994 .

[30]  Paige J. Novak,et al.  Biofilm Cohesiveness Measurement Using a Novel Atomic Force Microscopy Methodology , 2007, Applied and Environmental Microbiology.

[31]  Renaud Escudié,et al.  Stratification in the cohesion of biofilms grown under various environmental conditions. , 2008, Water research.

[32]  H. H. Fang,et al.  Quantification of bacterial adhesion forces using atomic force microscopy (AFM). , 2000, Journal of microbiological methods.

[33]  S. Molin,et al.  Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants , 2003, Molecular microbiology.

[34]  A. Vasella,et al.  Probing specific lectin-carbohydrate interactions using atomic force microscopy imaging and force measurements , 2003 .

[35]  Charles Soussen,et al.  Automated Force Volume Image Processing for Biological Samples , 2011, PloS one.

[36]  Z Lewandowski,et al.  Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. , 1999, Biotechnology and bioengineering.

[37]  E. Paul,et al.  Cohesion and detachment in biofilm systems for different electron acceptor and donors. , 2007, Water science and technology : a journal of the International Association on Water Pollution Research.

[38]  E. Kuffel,et al.  Formation of hydrophobic coating on glass surface using atmospheric pressure non-thermal plasma in ambient air , 2004 .

[39]  J. Block,et al.  Effect of wall shear rate on biofilm deposition and grazing in drinking water flow chambers , 2007, Biotechnology and bioengineering.

[40]  V. Körstgens,et al.  Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. , 2001, Water science and technology : a journal of the International Association on Water Pollution Research.

[41]  G. Hadziioannou,et al.  Entropic elasticity of single polymer chains of poly(methacrylic acid) measured by atomic force microscopy , 1999 .

[42]  S. Martin,et al.  The use of force-volume microscopy to examine bacterial attachment to titanium surfaces , 2010, Annals of Microbiology.

[43]  E. Dague,et al.  Surface Structure and Nanomechanical Properties of Shewanella putrefaciens Bacteria at Two pH values (4 and 10) Determined by Atomic Force Microscopy , 2005, Journal of bacteriology.

[44]  Zhibing Zhang,et al.  Bacterial adhesion and biofilms on surfaces , 2008 .

[45]  B. Olson,et al.  The occurrence of filamentous fungi in drinking water distribution systems. , 1982, Canadian Journal of Microbiology (print).

[46]  T. Camesano,et al.  Elasticity of Pseudomonas putida KT2442 Surface Polymers Probed with Single-Molecule Force Microscopy , 2002 .

[47]  J. Ghigo,et al.  Escherichia coli biofilms. , 2008, Current topics in microbiology and immunology.

[48]  Yves F Dufrêne,et al.  Nanostructure and nanomechanics of live Phaeodactylum tricornutum morphotypes. , 2008, Environmental microbiology.

[49]  Paul Stoodley,et al.  Viscoelasticity of Staphylococcus aureus Biofilms in Response to Fluid Shear Allows Resistance to Detachment and Facilitates Rolling Migration , 2005, Applied and Environmental Microbiology.

[50]  Y. Dufrêne,et al.  Direct Observation of Staphylococcus aureus Cell Wall Digestion by Lysostaphin , 2008, Journal of bacteriology.

[51]  R. Lévy,et al.  Measuring the spring constant of atomic force microscope cantilevers: thermal fluctuations and other methods , 2002 .

[52]  H. C. van der Mei,et al.  Retention of bacteria on a substratum surface with micro-patterned hydrophobicity. , 2000, FEMS microbiology letters.

[53]  S. D. De Keersmaecker,et al.  Detection, localization, and conformational analysis of single polysaccharide molecules on live bacteria. , 2008, ACS nano.

[54]  D. Cowan,et al.  Rapid detection of fungi in tissues using calcofluor white and fluorescence microscopy. , 1984, Archives of pathology & laboratory medicine.

[55]  J. Spurk Boundary Layer Theory , 2019, Fluid Mechanics.

[56]  V. Dupres,et al.  Structure, cell wall elasticity and polysaccharide properties of living yeast cells, as probed by AFM , 2008, Nanotechnology.

[57]  Claude Poleunis,et al.  Kinetics of conditioning layer formation on stainless steel immersed in seawater , 2001 .

[58]  J. Block,et al.  Probing young drinking water biofilms with hard and soft particles. , 2009, Water research.

[59]  Thomas J. Hanratty,et al.  Velocity gradients at the wall for flow around a cylinder at Reynolds numbers from 5 × 103 to 105 , 1969, Journal of Fluid Mechanics.

[60]  H. C. van der Mei,et al.  The Effect of Dissolved Organic Carbon on Bacterial Adhesion to Conditioning Films Adsorbed on Glass from Natural Seawater Collected during Different Seasons , 2003, Biofouling.